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Perspective Perspective Communicative & Integrative Biology 6:6, e26760; November/December 2013; © 2013 Landes Bioscience Evolutionary basins of attraction and convergence in plants and animals John Gardiner* The School of Biological Sciences; The University of Sydney; Camperdown, NSW Australia L iving organisms evolve, in part, according to the underlying properties of the amino acids and other compounds of which they are composed. Thus there are evolutionary basins of attraction that living organisms will tend to evolve toward. These processes are complex and probably beyond our current capabilities to fully envisage. But progress is being made toward an understanding of such principles by efforts to catalog protein folds and protein–protein interactions. Even plants and animals show convergent evolution, possibly driven by underlying evolutionary basins of attraction. Physical and chemical parameters and the properties of proteins present in the last common ancestor of these 2 taxa, including a putative connexin ancestor, may have played key roles here. Thus evolution is perhaps not as random as is sometimes depicted, but will follow predefined pathways. Here I address convergent evolution in plants and animals beginning at the molecular level and progressing to the organismic one. Introduction Keywords: attractor, evolution, protein folds, rebar, convergence *Correspondence to: John Gardiner; Email: [email protected] Submitted: 09/06/2013; Accepted: 10/09/2013 Citation: Gardiner J. Evolutionary basins of attraction and convergence in plants and animals. Communicative & Integrative Biology 2014; 7:e26760; http://dx.doi.org/10.4161/cib.26760 All lineages of living organisms are subject to evolutionary pressures that dictate that they are constantly evolving over time. From Weinreich et al. 2013:1 “In 1932 Sewall Wright introduced the notion of the fitness landscape. By analogy with a physical landscape, whose gradient predicts a rolling marble’s spatial trajectory, the contours of the fitness landscape are meant to predict an evolving population’s genetic trajectory.” A study on a computational model of protein folding and binding called “lattice proteins” discovered an important evolutionary principle related to the idea of the fitness landscape. “…the mutational landscape, the fitness landscape (binding process), and the genotype–phenotype map (folding process), together with the other scenario details, define a multi-dimensional set of evolutionary ‘pathways’ that the descendants of a given founder are likely to follow.”2 In addition, “Although these high-dimensional pathways are difficult for us to visualize, they are persistent across replicates of a given scenario. They describe basins of attraction that pull the lineages through the evolutionary process, to repeatable outcomes.” Similarly, another study on equilibrium in games3 states that “…the basic intuitions behind the calculations— that evolution with noise tends to favor limit sets with larger basins of attraction, and that the presence of intermediate steady states may facilitate evolution— each have predecessors in the literature. That a set with a large enough basin of attraction is selected has been noted in a number of places.” So what is a basin of attraction? An attractor is a set toward which a variable, moving according to the dictates of a dynamical system, evolves over time (Fig. 1). That is, points that get close enough to the attractor remain close even if slightly disturbed. For each such attractor, its basin of attraction is the set of initial conditions leading to long-time behavior that approaches that attractor. Attractors in 2 or 3 dimensions can be visualized (Fig. 1). Many attractors in biological evolution are extremely complex and therefore difficult to imagine. www.landesbioscience.comCommunicative & Integrative Biologye26702-1 the course of evolutionary history in plants and animals. Invasive cells (invadopodia of transformed metazoan cells, neurites, pollen tubes and fibers) in both plants and animals depend upon evolutionarily conserved machinery of cellular polarization and oriented cell mobilisation, involving the actin cytoskeleton and the secretory pathway. Connexins are proteins that form gap junctions between cells in animals. Earlier antibody studies indicated that there may be a conserved connexin homolog at the heart of plasmodesmata, connecting organelles between plant cells.7 Interestingly, performing BLAST protein homology searching between various animal connexins and the Arabidopsis thaliana proteome, cytochrome P450 proteins appear much more often than might be expected by chance alone. Thus this family of proteins may contain the elusive connexin homolog in plants. Indeed, a cytochrome P450 Figure 1. A Poisson attractor in 3 dimensions; even relatively simple attractors are complex. Evolutionary has already been shown to localize attractors are probably currently beyond our abilities to fully depict. to plasmodesmata.8 Armadillo/ catenin repeat proteins in animals All living organisms are composed of This means that there will be certain are involved in intercellular junction water, other compounds and elements evolutionary outcomes that are more formation in animals.9 In plants, an from both the a-biotic and biotic likely than others, or in other words, armadillo repeat protein links the environment, DNA, RNA, amino acids, evolutionary basins of attraction. In microtubule cytoskeleton to the cell wall and other compounds generated through addition to limits on the functions of via cellulose synthases, suggesting that the action of proteins composed of amino proteins, there are only a certain number this family of proteins has an intrinsic acids (through photosynthesis, predation, of ways it is physically possible to create ability to form such structures.10 saprofitic action, parasitism, symbiosis, a complex, multicellular organism. Here Protein products can drive convergent mutualism, and diffusion). Proteins have I explore how these evolutionary basins evolution an extremely large number of potential of attraction have caused convergence In neurons, serotonin is synthesized functions. Yet the range of their abilities is between plants and animals. The last from tryptophan in 2 steps involving not infinite. A recent study predicts that common ancestor of these 2 eukaryotic tryptophan hydroxylase and aromatic 2957 different protein folds are required lineages was unicellular, but there are amino acid decarboxylase. In plants, to cover all families in the Pfam protein many similarities in terms of multicellular serotonin is synthesized in 2 steps by database.4 The number of new protein organization, and other facets, between tryptophan decarboxylase converting families being discovered in the Pfam these 2 Kingdoms of organisms. These tryptophan to tryptamine followed by database is gradually reaching saturation. similarities stretch from the molecular the catalysis of tryptamine by tryptamine Another study predicts that there are only level to the organismic one. 5-hydroxylase to form serotonin.11 Thus, about 4000 possible types of protein– Protein preadaptation drives here, there has been convergent evolution protein interactions.5 convergence (to the synthesis of serotonin) but via 2 As an organism evolves, its phenotype Some proteins present in the last different biochemical pathways. This will be limited among other things by common ancestor of plant and animal demonstrates that sometimes evolutionary the bounds of protein function. Certain lineages appear to have preadaptation basins of attraction depend upon not important protein functions will only be to certain functions in multicellular so much the proteins involved but the possible through a small, perhaps even organisms. These proteins may then chemical products of those proteins. It unique, arrangement of amino acids. have “nucleated” certain structures over appears that serotonin is highly useful as e26702-2Communicative & Integrative BiologyVolume 6 Issue 6 a signaling molecule. In animals it is a major player in neural signaling, and there is an increasing body of work showing that it plays an important role in plant intercellular communication as well, possibly acting as a natural auxin inhibitor.12 Interestingly, serotonin is localized preferentially to vascular bundle companion cells and vascular parenchyma cells.13 This is of interest since it appears possible that plant vascular bundles perform a role in long-distance signaling similar to that of neurons in animals.14 Other chemical pathways have evolved independently in plants and animals. Some universal infochemicals used as nutrient indicators by saprophagous, coprophagous, and necrophagous insects have evolved in plants. These compounds mimic those found in animal carrion and are used by plants to attract insects for the purpose of pollination.15 It was proposed to simultaneously deter large herbivores.16 Plants and animals have also independently evolved similar pathways to the synthesis of cyanogenic glucosides as defense Figure 2. Steel rebar ready to be embedded in cast concrete. Note ridges on steel to help binding to compounds.17 concrete. Physical principles can drive convergent evolution Rebar, short for reinforcing bar, is a and therefore unidirectional glass fiber- leads to stunted plant inflorescences. common steel bar used as a tensioning reinforced thermoset resins are now being While it appears that the collapse xylem device in reinforced concrete and masonry. used in high-corrosion environments. vessels here may indicate that cellulose Here I suggest that, as is so often the case, These resins are available in many is important for compression resistance, nature has “invented” rebar long before structural forms, including spirals. and indeed wood is a strain-softening the human application of the practice, Xylem in plants as rebar substance20 similar to concrete,21 there and indeed the use of rebar by living Plants use xylem vessels to transport is evidence that cellulose in xylem is organisms has led to convergence in plant water and solutes from the root of the important in tension resistance as well.22 and animal lineages. During building, the plant to the aerial structure of the plant. Angiosperms develop tension wood bars are given ridges for better mechanical Xylem vessels are made of rigid cell wall on the upper side of drooping branches. anchoring into concrete (Fig. 2) because material, largely cellulose, and undergo Tension wood is characterized by the concrete is strong under compression apoptosis during development, losing development of a highly crystalline but relatively weak under tension. their cytoplasm so as to create empty cellulose-enriched gelatinous layer Steel is ideal for the reinforcement of tube-like structures. Xylem is important next to the lumen of the tension wood concrete as both substances have similar structurally as well, and indeed woody fibers, along with a reduction in lignin coefficients of thermal expansion, tissue is predominantly composed of (which is the principal compressionmeaning that reinforced concrete will xylem (Fig. 3). The irregular xylem (irx) resistant component of plant cell walls) not experience great stress as a result of mutants of Arabidopsis thaliana show and hemicellulose.23 The endoglucanase changes in temperature. Concrete is a collapsed xylem vessels as a result of KORRIGAN, which is involved in strain-softening substance while the reduced amounts of cellulose, lignin, or cellulose deposition, and 3 xylem-specific steel reinforcement is strain-hardening.18 other cell wall components.19 irx stems cellulose synthases are all highly expressed Steel can be subject to rust, however, are also structurally weaker, and this in developing tension wood.24 Thus www.landesbioscience.comCommunicative & Integrative Biologye26702-3 Figure 3. Image showing various cell wall forms in plants, including secondary cell wall forms of xylem vessels. Image downloaded from Florida Center for Instructional Technology website. Figure 4. Sponge spicules of various forms. Image downloaded from Florida Center for Instructional Technology website. cellulose-enriched xylem appears likely to act as rebar during wood development. Indeed the structure of xylem vessels is even reminiscent of steel rebar structure (Fig. 3). Some plants, including Gnetum gnemon, have extraxylary gelatinous tension fibers25 that may function as cellular rebar. Spicules in animals as rebar Small pieces of calcareous or siliceous material are embedded in sponges as spicules, in cnidarians as sclerites, and as spicules in chitons, stalked barnacles, and ascidians. Sponge spicules are probably the best studied of this group. It is known that bio-silica is synthesized via the protein silicatein, which aggregates non-covalently to form larger filaments, a process that is stabilized by the silicatein-associated protein silintaphin-1. These structured clusters form the axial filament that is located in the center of the spicules, the axial canal.26 Spicules can be quite long—the anchoring spicule of the sponge Monoraphis is up to a meter in length and several millimeters in diameter. When compared with a silica rod of the same size, the spicule is able to withstand a 4-fold higher stress before breaking due to its layered structure. Spicules with very high aspect ratios appear to act like rebar; stress is transferred by shearing from the pliable matrix to the stiff fibers, which thus bear in tension part of the load on the composite.27 Indeed spicules come in a variety of shapes, some of which involve hooks at the ends of the spicules that may have a similar role to hooks or bends at the ends of steel rebar that lock it around the concrete (Fig. 4). The parallel phenomenon in plants is branched sclereids in the soft tissue of nymphaea leaves. Murray’s law Two related “living fossil” plants, Tmesipteris and Psilotum, are found in Australia and other parts of the world. Due to its being more widely dispersed, most scientific work on this family of ancient plants, the Psilotaceae, has been performed on Psilotum. The xylem of Psilotum nudum does not provide structural support to the plant, unlike more modern plant lineages where disruption of xylem leads to stunted growth. The lack of mechanical support e26702-4Communicative & Integrative BiologyVolume 6 Issue 6 by the xylem of Psilotum has enabled an examination and confirmation of Murray’s law for plant xylem vessels. Murray’s law states that, as vessels branch, the sum of the conduit radii cubed at any point along the plant should decrease in direct proportion with volume flow rate to maximize hydraulic conductance per unit vascular investment.28 Murray’s law also governs the branching of blood vessels in animals.29 Thus Murray’s law has replaced earlier models of hydraulic conductance in a branched transport system including the pipe model and Leonardo’s rule.30 Here again physical principles have dictated convergent evolution between plant and animal lineages. References 11. Park S, Byeon Y, Back K. Transcriptional suppression of tryptamine 5-hydroxylase, a terminal serotonin biosynthetic gene, induces melatonin biosynthesis in rice (Oryza sativa L.). J Pineal Res 2013; 55:131-7; PMID:23521226; http://dx.doi.org/10.1111/jpi.12053 12. Pelagio-Flores R, Ortíz-Castro R, Méndez-Bravo A, Macías-Rodríguez L, López-Bucio J. Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in Arabidopsis thaliana. Plant Cell Physiol 2011; 52:490-508; PMID:21252298; http://dx.doi.org/10.1093/pcp/ pcr006 13. Kang K, Kim Y-S, Park S, Back K. Senescenceinduced serotonin biosynthesis and its role in delaying senescence in rice leaves. Plant Physiol 2009; 150:138093; PMID:19439571; http://dx.doi.org/10.1104/ pp.109.138552 14. Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM, et al. The plant vascular system: evolution, development and functions. J Integr Plant Biol 2013; 55:294-388; PMID:23462277; http://dx.doi. org/10.1111/jipb.12041 15. Jürgens A, Wee SL, Shuttleworth A, Johnson SD. Chemical mimicry of insect oviposition sites: a global analysis of convergence in angiosperms. Ecol Let 2013; http://dx.doi.org/10.1111/ele.12152. 16. Lev-Yadun S, Ne’eman G, Shanas U. A sheep in wolf’s clothing: do carrion and dung odours of flowers not only attract pollinators but also deter herbivores? Bioessays 2009; 31:84-8; PMID:19154006; http:// dx.doi.org/10.1002/bies.070191 17. Jensen NB, Zagrobelny M, Hjernø K, Olsen CE, Houghton-Larsen J, Borch J, Møller BL, Bak S. Convergent evolution in biosynthesis of cyanogenic defence compounds in plants and insects. Nat Commun 2011; 2:273; PMID:21505429; http:// dx.doi.org/10.1038/ncomms1271 18. Koehl MAR. Mechanical design of spicule-reinforced connective tissue stiffness. J Exp Biol 1982; 98:239-67 19. Turner SR, Somerville CR. Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 1997; 9:689-701; PMID:9165747 20. Miyauchi K, Murata K. Strain-softening behavior of wood under tension perpendicular to the grain. J Wood Sci 2007; 53:463-9; http://dx.doi.org/10.1007/ s10086-007-0899-3 21. Carpinteri A. Applications of fracture mechanics to reinforced concrete. New York, NY: Elsevier Science Publishing Co, 1992 1. Weinreich DM, Sindi S, Watson RA. Finding the boundary between evolutionary basins of attraction, and implications for Wright’s fitness landscape analogy. J Stat Mech Theory Exp 2013; P01001; http://dx.doi. org/10.1088/1742-5468/2013/01/P01001. 2. Palmer ME, Moudgil A, Feldman MW. Longterm evolution is surprisingly predictable in lattice proteins. J R Soc Interface 2013; 10:20130026; PMID:23466559; http://dx.doi.org/10.1098/ rsif.2013.0026 3. Ellison G. Basins of Attraction, Long-Run Stochastic Stability, and the Speed of Step-by-Step Evolution. Rev Econ Stud 2000; 67:17-45; http://dx.doi. org/10.1111/1467-937X.00119 4. Liu X, Lv B, Guo W. The size distribution of protein families within different types of folds. Biochem Biophys Res Commun 2011; 406:21822; PMID:21303659; http://dx.doi.org/10.1016/j. bbrc.2011.02.020 5. Garma L, Mukherjee S, Mitra P, Zhang Y. How many protein-protein interactions types exist in nature? PLoS One 2012; 7:e38913; PMID:22719985; http:// dx.doi.org/10.1371/journal.pone.0038913 6. Vaškovičová K, Žárský V, Rösel D, Nikolič M, Buccione R, Cvrčková F, Brábek J. Invasive cells in animals and plants: searching for LECA machineries in later eukaryotic life. Biol Direct 2013; 8:8; PMID:23557484; http://dx.doi. org/10.1186/1745-6150-8-8 7. Meiners S, Xu A, Schindler M. Gap junction protein homologue from Arabidopsis thaliana: evidence for connexins in plants. Proc Natl Acad Sci U S A 1991; 88:4119-22; PMID:1851993; http://dx.doi. org/10.1073/pnas.88.10.4119 8. Escobar NM, Haupt S, Thow G, Boevink P, Chapman S, Oparka K. High-throughput viral expression of cDNA-green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. Plant Cell 2003; 15:1507-23; PMID:12837943; http://dx.doi. org/10.1105/tpc.013284 9. Valenta T, Hausmann G, Basler K. The many faces and functions of β-catenin. EMBO J 2012; 31:271436; PMID:22617422; http://dx.doi.org/10.1038/ emboj.2012.150 10. Mei Y, Gao HB, Yuan M, Xue HW. The Arabidopsis ARCP protein, CSI1, which is required for microtubule stability, is necessary for root and anther development. Plant Cell 2012; 24:1066-80; PMID:22427339; http://dx.doi.org/10.1105/tpc.111.095059 Conclusions Evolution is a multi-faceted process. There are many variables to consider, and a full understanding of how it works is probably currently not possible. Convergence is one theme that appears time and time again. Even plants and animals, 2 very divergent lineages, show certain convergences. Within the taxa of plants or animals, there are even more instances of convergent evolution. These appear likely to be due to evolutionary basins of attraction that are in turn dependent upon the chemical and physical properties of the components of living organisms and other physical considerations. Thus evolution is not a random process but has led to certain outcomes that were, to a certain extent at least, preordained. Disclosure of Potential Conflicts of Interest No potential conflicts of interest were disclosed. 22. Eckardt NA. Cellulose synthesis takes the CesA train. Plant Cell 2003; 15:1685-7; http://dx.doi. org/10.1105/tpc.150810 23. Andersson-Gunnerås S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B. Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 2006; 45:144-65; PMID:16367961; http://dx.doi. org/10.1111/j.1365-313X.2005.02584.x 24. Bhandari S, Fujino T, Thammanagowda S, Zhang D, Xu F, Joshi CP. Xylem-specific and tension stress-responsive coexpression of KORRIGAN endoglucanase and three secondary wall-associated cellulose synthase genes in aspen trees. Planta 2006; 224:828-37; PMID:16575593; http://dx.doi. org/10.1007/s00425-006-0269-1 25. Tomlinson PB. Development of gelatinous (reaction) fibers in stems of Gnetum gnemon (Gnetales). Am J Bot 2003; 90:965-72; PMID:21659194; http:// dx.doi.org/10.3732/ajb.90.7.965 26. Wang X, Müller WE. Complex structures – smart solutions: Formation of siliceous spicules. Commun Integr Biol 2011; 4:684-8; PMID:22446527 27. Koehl MAR. Mechanical design of spiculereinforced connective tissue stiffness. J Exp Biol 1982; 98:239-67 28. McCulloh KA, Sperry JS. The evaluation of Murray’s law in Psilotum nudum (Psilotaceae), an analogue of ancestral vascular plants. Am J Bot 2005; 92:985-9; PMID:21652482; http://dx.doi. org/10.3732/ajb.92.6.985 29. Painter PR, Edén P, Bengtsson HU. Pulsatile blood flow, shear force, energy dissipation and Murray’s Law. Theor Biol Med Model 2006; 3:31; PMID:16923189; http://dx.doi. org/10.1186/1742-4682-3-31 30. McCulloh KA, Sperry JS, Adler FR. Water transport in plants obeys Murray’s law. Nature 2003; 421:93942; PMID:12607000; http://dx.doi.org/10.1038/ nature01444 www.landesbioscience.comCommunicative & Integrative Biologye26702-5